Punishers Benefit From Third-Party
Punishment in Fish
Nichola J. Raihani,1* Alexandra S. Grutter,2Redouan Bshary3
H
uman studies show that uninvolvedby-standers often pay to punish defectors (1, 2). Such behavior has typically been interpreted in terms of group-level benefits (3) despite theoretical predictions that third-party ishment can yield individual benefits to the pun-isher (4). Here, we show that male cleaner fish, Labroides dimidiatus, punish their female part-ners if females cheat while inspecting model clients. Punishment promotes female cooperation, yielding direct foraging benefits to the male. This finding demonstrates empirically that third-party punishment can evolve via self-serving tendencies. When servicing clients, cleaners either coop-erate by removing ectoparasites or cheat by taking a bite of mucus. Cleaners prefer to eat mucus (5) but risk clients terminating the interaction if they do (6). The conflict of interest between cleaner and client is less pronounced during inspections by cleaner pairs than during singleton inspections (7). Increased service quality during pair inspec-tions was interpreted as resulting from female cooperation, both under natural conditions and in the laboratory where Plexiglas (acrylic plastic) plates serve as model clients. Larger males reg-ularly chased smaller female partners if females caused clients to leave, particularly in the labo-ratory (7). This male behavior is peculiar because clients, not males, are the victims of biting fe-males. Despite this fact, it is possible that male chasing could cause females to behave more co-operatively in future interactions. If males benefit
personally through increased foraging success, then the males’ behavior represents third-party punishment that evolves via self-regarding, rather than altruistic, tendencies.
Cleaners were trained to feed off model clients (Plexiglas plates) containing two food types: pre-ferred prawn and less-prepre-ferred fish flake (8). Eat-ing prawn corresponded to cheatEat-ing the client by eating mucus, whereas eating flake corresponded to cooperating by removing ectoparasites. Eating prawn resulted in the immediate removal of the plate. We replicated earlier results (7) that males more often chased females when the latter’s be-havior caused plate removal (Wilcoxon signed-rank test, n = 8, V (signed-rank sum of positive values of x = y) = 21, P = 0.036). After being chased, females were less likely to eat prawn again in the second plate presentation 60 s later (Wilcoxon signed-rank test, n = 8, V = 34, P = 0.030; Fig. 1A) and fed against their preference, eating a higher ratio of flake to prawns (Wilcoxon signed-rank test, n = 8, V = 36, P = 0.008; Fig. 1B). This allowed males to increase their food intake in the second presentation (Wilcoxon signed-rank test, n = 8, V = 28, P = 0.02; Fig. 1C). Conversely, when chasing was prevented with a temporary partition, females that cheated in the first pre-sentation were equally likely to cheat in the second one (Wilcoxon signed-rank test, n = 8, V = 11, P = 0.67; Fig. 1A) and did not eat a higher ratio of flake to prawn items (Wilcoxon signed-rank test, n = 8, V = 8, P = 0.35; Fig. 1B),
and male foraging efficiency did not improve (Wilcoxon signed-rank test, n = 8, V = 17.5, P = 1.0; Fig. 1C). In nature, male cleaners may bene-fit if they punish cheating females, even though clients are the primary victims. The establishment of self-serving third-party punishment in response to personal losses may be a key step toward third-party punishment without current involvement as in humans (2).
References and Notes
1. E. Fehr, U. Fischbacher, Evol. Hum. Behav. 25, 63 (2004).
2. E. Fehr, S. Gächter, Nature 415, 137 (2002). 3. R. Boyd, H. Gintis, S. Bowles, P. J. Richerson, Proc. Natl.
Acad. Sci. U.S.A. 100, 3531 (2003). 4. K. Jaffe, Acta Biotheor. 52, 155 (2004).
5. A. S. Grutter, R. Bshary, Proc. Biol. Sci. 270 (suppl. 2), S242 (2003).
6. R. Bshary, A. S. Grutter, Anim. Behav. 63, 547 (2002). 7. R. Bshary, A. S. Grutter, A. S. T. Willener, O. Leimar,
Nature 455, 964 (2008).
8. Materials and methods are available as supporting material on Science Online.
9. We thank M. Cant, A. Ridley, and A. Thornton for commenting on earlier versions of this manuscript and L. Brun, A. Bshary, A. Pinto, D. Rappaz, and M. Soares for assistance in the field. N.J.R. is funded by the Zoological Society of London, R.B. by the Swiss Science Foundation, and A.S.G. by the University of Queensland.
1
Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK.2Institut de Biologie, Universitè
de Neuchâtel, CH-2009 Neuchâtel, Switzerland.3School of
Biological Sciences, The University of Queensland, Brisbane Qld 4072, Australia.
*To whom correspondence should be addressed. E-mail: [email protected]
male chased female chasing prevented
Difference in number of prawn items
eaten by female -0 .3 -0 .2 -0 .1 0.0 0 .1 0.2 0 .3 A
male chased female chasing prevented
Difference in flake:prawn eaten by female
-3 -2 -1 0 1 2 3 B
male chased female chasing prevented
Difference in total items eaten by male
-0 .4 -0 .2 0.0 0 .2 0.4 0 .6 0.8 1 .0 C
Fig. 1. Median difference according to treatment in (A) the number of prawn items eaten by females, (B) the ratio of flake to prawn items eaten by females, and (C) the total number of food items eaten by the male. For each pair, we first calculated (A) mean number of prawn items female ate, (B) mean ratio of flake to prawn items female ate, and (C) mean number of food items
male ate in first and second presentations, respectively. Differences for each pair were calculated by subtracting mean (presentation one) from mean (presentation two). The median of these differences and the interquartile range were then calculated and are presented in the figure (gray boxes and bars, respectively).
Published in Science 327, no 5962, 171, 2010
